Neutrophils express oncomodulin and promote optic nerve regeneration

Journal of Neuroscience

Volumn 33, Issue 37, 2013, Pages 14816-14824

  Kurimoto, Takuji ^a,b,c   Yin, Yuqin ^a,c   Habboub, Ghaith ^a,c   Gilbert, Hui Ya ^a   Li, Yiqing ^a,c   Nakao, Shintaro ^c   Hafezi Moghadam, Ali ^c   Benowitz, Larry I ^a,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b OSAKA MEDICAL COLLEGE   (Japan)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; INTERLEUKIN 6; LEUKEMIA INHIBITORY FACTOR; ONCOMODULIN; PEPTIDE HORMONE ANTAGONIST;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL SURVIVAL; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE; MALE; MOUSE; NERVE REGENERATION; NEUTROPHIL; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ANTIGENS, CD; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; CILIARY NEUROTROPHIC FACTOR; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERLEUKIN-6; LEUKEMIA INHIBITORY FACTOR; MALE; MICE; MICE, INBRED C57BL; NERVE CRUSH; NERVE REGENERATION; NEUTROPHILS; OPTIC NERVE DISEASES; RECEPTORS, CELL SURFACE; RETINA; RETINAL GANGLION CELLS; STILBAMIDINES; VISUAL PATHWAYS;

EID: 84883677922     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5511-12.2013     Document Type: Article

References (53)

1. Austyn JM, Gordon S (1981) F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol 11:805-815. CrossRef Medline
2. Barrette B, Hébert MA, Filali M, Lafortune K, Valliéres N, Gowing G, Julien JP, Lacroix S, (2008) Requirement of myeloid cells for axon regeneration. J Neurosci 28:9363-9376. CrossRef Medline
3. Benowitz LI, Popovich PG (2011) Inflammation and axon regeneration. Curr Opin Neurol 24:577-583. CrossRef Medline
4. Brinkmann V, Zychlinsky A (2012) Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 198:773-783. CrossRef Medline
5. Carlson SL, Parrish ME, Springer JE, Doty K, Dossett L (1998) Acute inflammatory response in spinal cord following impact injury. Exp Neurol 151:77-88. CrossRef Medline
6. Cen LP, Luo JM, Zhang CW, Fan YM, Song Y, So KF, van Rooijen N, Pang CP, Lam DS, Cui Q (2007) Chemotactic effect of ciliary neurotrophic factor on macrophages in retinal ganglion cell survival and axonal regeneration. Invest Ophthalmol Vis Sci 48:4257-4266. CrossRef Medline
7. Chen Q, Smith GM, Shine HD (2008) Immune activation is required for NT-3-induced axonal plasticity in chronic spinal cord injury. Exp Neurol 209:497-509. CrossRef Medline
8. Cohen A, Bray GM, Aguayo AJ (1994) Neurotrophin-4/5 (NT-4/5) increases adult rat retinal ganglion cell survival and neurite outgrowth in vitro. J Neurobiol 25:953-959. CrossRef Medline
9. Cui Q, Yip HK, Zhao RC, So KF, Harvey AR (2003) Intraocular elevation of cyclic AMP potentiates ciliary neurotrophic factor-induced regeneration of adult rat retinal ganglion cell axons. Mol Cell Neurosci 22:49-61. CrossRef Medline
10. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE (2008) Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 83:64-70.
11. de Lima S, Koriyama Y, Kurimoto T, Oliveira JT, Yin Y, Li Y, Gilbert HY, Fagiolini M, Martinez AM, Benowitz L (2012) Full-length axon regeneration in the adult mouse optic nerve and partial recovery of simple visual behaviors. Proc Natl Acad Sci U S A 109:9149-9154. CrossRef Medline
12. De Resende MM, Stodola TJ, Greene AS (2010) Role of the renin angiotensin system on bone marrow-derived stem cell function and its impact on skeletal muscle angiogenesis. Physiol Genomics 42:437-444. CrossRef Medline
13. Donnelly DJ, Popovich PG (2008) Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp Neurol 209:378-388. CrossRef Medline
14. Dusart I, Schwab ME (1994) Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci 6:712-724. CrossRef Medline
15. Fischer D, Pavlidis M, Thanos S (2000) Cataractogenic lens injury prevents traumatic ganglion cell death and promotes axonal regeneration both in vivo and in culture. Invest Ophthalmol Vis Sci 41:3943-3954. Medline
16. Fischer D, Petkova V, Thanos S, Benowitz LI (2004) Switching mature retinal ganglion cells to a robust growth state in vivo: gene expression and synergy with RhoA inactivation. J Neurosci 24:8726-8740. CrossRef Medline
17. Fischer D, Hauk TG, Müller A, Thanos S (2008) Crystallins of the beta/ gamma-superfamily mimic the effects of lens injury and promote axon regeneration. Mol Cell Neurosci 37:471-479. CrossRef Medline
18. Fleming TJ, Fleming ML, Malek TR (1993) Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow. RB6-8C5 mAb to granulocyte-differentiation antigen (Gr-1) detects members of the Ly-6 family. J Immunol 151:2399-2408. Medline
19. Gensel JC, Nakamura S, Guan Z, van Rooijen N, Ankeny DP, Popovich PG (2009) Macrophages promote axon regeneration with concurrent neurotoxicity. J Neurosci 29:3956-3968. CrossRef Medline
20. Gillen MF, Banville D, Rutledge RG, Narang S, Seligy VL, Whitfield JF, Mac- Manus JP (1987) A complete complementary DNA for the oncodevelopmental calcium-binding protein, oncomodulin. J Biol Chem 262: 5308-5312. Medline
21. Hauk TG, Müller A, Lee J, Schwendener R, Fischer D (2008) Neuroprotective and axon growth promoting effects of intraocular inflammation do not depend on oncomodulin or the presence of large numbers of activated macrophages. Exp Neurol 209:469-482. CrossRef Medline
22. Hauk TG, Leibinger M, Müller A, Andreadaki A, Knippschild U, Fischer D (2010) Intravitreal application of the Toll-like receptor 2 agonist Pam3Cys stimulates axon regeneration in the mature optic nerve. Invest Ophthalmol Vis Sci 51:459-464. CrossRef Medline
23. Hestdal K, Ruscetti FW, Ihle JN, Jacobsen SE, Dubois CM, Kopp WC, Longo DL, Keller JR (1991) Characterization and regulation of RB6-8C5 antigen expression on murine bone marrow cells. J Immunol 147:22-28. Medline
24. Horn KP, Busch SA, Hawthorne AL, van Rooijen N, Silver J (2008) Another barrier to regeneration in the CNS: activated macrophages induce extensive retraction of dystrophic axons through direct physical interactions. J Neurosci 28:9330-9341. CrossRef Medline
25. Kurimoto T, Yin Y, Omura K, Gilbert HY, Kim D, Cen LP, Moko L, Kügler S, Benowitz LI (2010) Long-distance axon regeneration in the mature optic nerve: contributions of oncomodulin, cAMP, and pten gene deletion. J Neurosci 30:15654-15663. CrossRef Medline
26. Lawson LJ, Perry VH, Dri P, Gordon S (1990) Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39:151-170. CrossRef Medline
27. Leaver SG, Cui Q, Plant GW, Arulpragasam A, Hisheh S, Verhaagen J, Harvey AR (2006) AAV-mediated expression of CNTF promotes long-term survival and regeneration of adult rat retinal ganglion cells. Gene Ther 13:1328-1341. CrossRef Medline
28. Leibinger M, Müller A, Andreadaki A, Hauk TG, Kirsch M, Fischer D (2009) Neuroprotective and axon growth-promoting effects following inflammatory stimulation on mature retinal ganglion cells in mice depend on ciliary neurotrophic factor and leukemia inhibitory factor. J Neurosci 29:14334-14341. CrossRef Medline
29. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI (2000) Lens injury stimulates axon regeneration in the mature rat optic nerve. J Neurosci 20:4615-4626. Medline
30. Li S, Li T, Luo Y, Yu H, Sun Y, Zhou H, Liang X, Huang J, Tang S (2011) Retro-orbital injection of FITC-dextran is an effective and economical method for observing mouse retinal vessels. Mol Vis 17:3566-3573. Medline
31. Li Y, Irwin N, Yin Y, Lanser M, Benowitz LI (2003) Axon regeneration in goldfish and rat retinal ganglion cells: differential responsiveness to carbohydrates and cAMP. J Neurosci 23:7830-7838. Medline
32. Lingor P, Tönges L, Pieper N, Bermel C, Barski E, Planchamp V, Bähr M (2008) ROCK inhibition and CNTF interact on intrinsic signalling pathways and differentially regulate survival and regeneration in retinal ganglion cells. Brain 131:250-263. Medline
33. Logan A, Ahmed Z, Baird A, Gonzalez AM, Berry M (2006) Neurotrophic factor synergy is required for neuronal survival and disinhibited axon regeneration after CNS injury. Brain 129:490-502. Medline
34. Lorber B, Berry M, Douglas MR, Nakazawa T, Logan A (2009) Activated retinal glia promote neurite outgrowth of retinal ganglion cells via apolipoprotein E. J Neurosci Res 87:2645-2652. CrossRef Medline
35. Lu X, Richardson PM (1991) Inflammation near the nerve cell body enhances axonal regeneration. J Neurosci 11:972-978. Medline
36. MacManus JP, Brewer LM (1987) Isolation, localization, and properties of the oncodevelopmental calcium-binding protein oncomodulin. Methods Enzymol 139:156-168. CrossRef Medline
37. MacManus JP, Whitfield JF, Boynton AL, Durkin JP, Swierenga SH (1982) Oncomodulin-a widely distributed, tumour-specific, calcium-binding protein. Oncodev Biol Med 3:79-90. Medline
38. Nadeau S, Filali M, Zhang J, Kerr BJ, Rivest S, Soulet D, Iwakura Y, de Rivero Vaccari JP, Keane RW, Lacroix S (2011) Functional recovery after peripheral nerve injury is dependent on the pro-inflammatory cytokines IL-1β and TNF: implications for neuropathic pain. J Neurosci 31:12533-12542. CrossRef Medline
39. Nathan C (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6:173-182. CrossRef Medline
40. Park KK, Hu Y, Muhling J, Pollett MA, Dallimore EJ, Turnley AM, Cui Q, Harvey AR (2009) Cytokine-induced SOCS expression is inhibited by cAMP analogue: impact on regeneration in injured retina. Mol Cell Neurosci 41:313-324. CrossRef Medline
41. Pernet V, Di PoloA (2006) Synergistic action of brain-derived neurotrophic factor and lens injury promotes retinal ganglion cell survival, but leads to optic nerve dystrophy in vivo. Brain 129:1014-1026. CrossRef Medline
42. Popovich PG, Longbrake EE (2008) Can the immune system be harnessed to repair the CNS? Nat Rev Neurosci 9:481-493. CrossRef Medline
43. Schnell L, Fearn S, Klassen H, Schwab ME, Perry VH (1999) Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur J Neurosci 11:3648-3658. CrossRef Medline
44. Schwartz M, Yoles E (2006) Immune-based therapy for spinal cord repair: autologous macrophages and beyond. J Neurotrauma 23:360-370. CrossRef Medline
45. Sica A, Rubino L, Mancino A, Larghi P, Porta C, Rimoldi M, Solinas G, Locati M, Allavena P, Mantovani A (2007) Targeting tumour-associated macrophages. Expert Opin Ther Targets 11:1219-1229. CrossRef Medline
46. Smith PD, Sun F, Park KK, Cai B, Wang C, Kuwako K, Martinez-Carrasco I, Connolly L, He Z (2009) SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron 64:617-623. CrossRef Medline
47. Steinmetz MP, Horn KP, Tom VJ, Miller JH, Busch SA, Nair D, Silver DJ, Silver J (2005) Chronic enhancement of the intrinsic growth capacity of sensory neurons combined with the degradation of inhibitory proteoglycans allows functional regeneration of sensory axons through the dorsal root entry zone in the mammalian spinal cord. J Neurosci 25:8066-8076. CrossRef Medline
48. Stirling DP, Liu S, Kubes P, Yong VW (2009) Depletion of Ly6G/Gr-1 leukocytes after spinal cord injury in mice alters wound healing and worsens neurological outcome. J Neurosci 29:753-764. CrossRef Medline
49. Tepper RI, Coffman RL, Leder P (1992) An eosinophil-dependent mechanism for the antitumor effect of interleukin-4. Science 257:548-551. CrossRef Medline
50. Weise J, Isenmann S, Klöcker N, Kügler S, Hirsch S, Gravel C, Bähr M (2000) Adenovirus-mediated expression of ciliary neurotrophic factor (CNTF) rescues axotomized rat retinal ganglion cells but does not support axonal regeneration in vivo. Neurobiol Dis 7:212-223. CrossRef Medline
51. Yin Y, Cui Q, Li Y, Irwin N, Fischer D, Harvey AR, Benowitz LI (2003) Macrophage-derived factors stimulate optic nerve regeneration. J Neurosci 23:2284-2293. Medline
52. Yin Y, Henzl MT, Lorber B, Nakazawa T, Thomas TT, Jiang F, Langer R, Benowitz LI (2006) Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat Neurosci 9:843-852. CrossRef Medline
53. Yin Y, Cui Q, Gilbert HY, Yang Y, Yang Z, Berlinicke C, Li Z, Zaverucha-do-Valle C, He H, Petkova V, Zack DJ, Benowitz LI (2009) Oncomodulin links inflammation to optic nerve regeneration. Proc Natl Acad Sci U S A 106:19587-19592. CrossRef Medline